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European Seahorse Taxonomy, Population Structure, and Habitat Use As a Basis for Assessment, Monitoring and Conservation

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European Seahorse Taxonomy, Population Structure, and Habitat Use As a Basis for Assessment, Monitoring and Conservation Marine Biology (2018) 165:19 https://doi.org/10.1007/s00227-017-3274-y ORIGINAL PAPER A synthesis of European seahorse taxonomy, population structure, and habitat use as a basis for assessment, monitoring and conservation Lucy C. Woodall1,2 · Francisco Otero‑Ferrer3 · Miguel Correia2,4 · Janelle M. R. Curtis5 · Neil Garrick‑Maidment6 · Paul W. Shaw7 · Heather J. Koldewey2,8 Received: 15 August 2017 / Accepted: 22 November 2017 © The Author(s) 2017. This article is an open access publication Abstract Accurate taxonomy, population demography, and habitat descriptors inform species threat assessments and the design of efective conservation measures. Here we combine published studies with new genetic, morphological and habitat data that were collected from seahorse populations located along the European and North African coastlines to help inform manage- ment decisions for European seahorses. This study confrms the presence of only two native seahorse species (Hippocampus guttulatus and H. hippocampus) across Europe, with sporadic occurrence of non-native seahorse species in European waters. For the two native species, our fndings demonstrate that highly variable morphological characteristics, such as size and pres- ence or number of cirri, are unreliable for distinguishing species. Both species exhibit sex dimorphism with females being signifcantly larger. Across its range, H. guttulatus were larger and found at higher densities in cooler waters, and individuals in the Black Sea were signifcantly smaller than in other populations. H. hippocampus were signifcantly larger in Senegal. Hippocampus guttulatus tends to have higher density populations than H. hippocampus when they occur sympatrically. Although these species are often associated with seagrass beds, data show both species inhabit a wide variety of shallow habitats and use a mixture of holdfasts. We suggest an international mosaic of protected areas focused on multiple habitat types as the frst step to successful assessment, monitoring and conservation management of these Data Defcient species. Introduction The paucity of species-specifc data is among the many chal- lenges to designing efective marine conservation measures Responsible Editor: K. D. Clements. that are resilient to the enduring threats of climate change, coastal development, over-fshing, by-catch efects and inva- Reviewed by R. Calado and an undisclosed expert. sive species (Klein et al. 2013; Selig et al. 2014). These challenges are further compounded when the taxonomy Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00227-017-3274-y) contains of species is uncertain. Knowing which species occur and supplementary material, which is available to authorized users. * Lucy C. Woodall 5 Pacifc Biological Station, Fisheries and Oceans Canada, [email protected] 3190 Hammond Bay Road, Nanaimo, BC, Canada 6 The Seahorse Trust, 36 Greatwood Terrace, Topsham, 1 Department of Zoology, University of Oxford, Oxford, UK Devon, UK 2 Project Seahorse, Zoological Society of London, Regent’s 7 Institute of Biological, Environmental and Rural Sciences Park, London, UK (IBERS), Aberystwyth University, Aberystwyth, UK 3 Grupo en Biodiversidad y Conservación, IU-ECOAQUA, 8 Centre for Ecology and Conservation, University of Exeter, Universidad de Las Palmas de Gran Canaria, Crta. Taliarte Penryn, UK s/n, 35214 Telde, Spain 4 CCMar, Universidade do Algarve, F. C. T., Edifcio 7, Campus de Gambelas, 8005‑139 Faro, Portugal Vol.:(0123456789)1 3 19 Page 2 of 19 Marine Biology (2018) 165:19 understanding their life-history, ecology, and behaviour is currently targeted by fsheries throughout most of their geo- increasingly important to ensure efective and robust con- graphic range, but there is trade in west Africa of H. hip- servation and management (Perry et al. 2005; Lavergne et al. pocampus (Cisneros-Montemayor et al. 2016) and a new and 2010; Dawson et al. 2011). increasing fshery for H. guttulatus in the Ria Formosa in The cryptic nature of seahorses (genus Hippocampus) has Portugal (M. Correia, pers. obs.). Both species are also sus- led to signifcant confusion regarding their taxonomy and ceptible to anthropogenic activities and habitat loss (Curtis ecology, which poses challenges to managing the activities et al. 2007). Ecological data on seahorses are scarce due to that threaten these fshes. The most recent and comprehen- their apparent patchy distribution and low density, as well sive taxonomic review suggests there are two native species as their cryptic nature (Foster and Vincent 2004). These fea- of seahorse in European waters, H. guttulatus and H. hip- tures make them particularly difcult to survey, assess and pocampus (Lourie et al. 2016), but considerable intraspecifc monitor the status of their populations, either for scientifc variability in morphology within this genus (Lourie et al. research or commercial development projects, such as envi- 1999b; Otero-Ferrer et al. 2017) has led to much confusion ronmental impact assessments prior to construction work. regarding their taxonomy, and the taxonomy and nomen- To date, a range-wide ecological assessment has been clature of these species is not stable. Authors previously conducted for just one seahorse species (H. capensis), which suggested many additional species within this geographic is confned to three estuaries in South Africa (Lockyear et al. range, based on small morphometric diferences (Kuiter 2006). For European seahorses, research has generally been 2009). For instance a study by Vasil’Eva (2007), which has limited to small focal sites (e.g. Curtis and Vincent 2006; not been adopted (Eschmeyer and Fricke 2016), attempted to Gristina et al. 2015) or collection of qualitative data (e.g. change the names of these species, while another author sug- Filiz and Taskavak 2012). However, a very large sighting gested additional species were present based on photographs dataset has been collected for UK and Ireland (N. Garrick- (Kuiter 2009). There is ongoing discussion as to whether Maidment pers. comm.). Comparisons of population struc- H. ramulosus is a simple synonym of H. guttulatus, and ture among studies is also challenging because seahorse whether the regional morphological diferences observed length can be measured by standard length (LS), total length across the seahorse populations in the region are indica- (LT) or height (Lourie et al. 1999a) and previous studies have tive of diferent species (Kuiter 2009). Taxonomic contro- used all of these (e.g. Verdiell-Cubedo et al. 2008; Nadeau versy involving splitting and lumping of species is common et al. 2009; Caldwell and Vincent 2012; Vieira et al. 2014). throughout the Syngnathidae family, due to limited discrimi- Focusing on the taxonomy, biology and life history of nating morphological characteristics between species and European seahorses, we use published and unpublished the ability within the family to change colour and cirri (fla- sources of genetic, demographic and environmental data to mentous skin appendages) (Curtis 2006). As most ecological investigate the following objectives: studies of seahorses in Europe have used the nomenclature of H. hippocampus and H. guttulatus to defne their focal 1. Use genetic markers to confrm the number of seahorse species (e.g. Curtis and Vincent 2005; Kitsos et al. 2008; species present in Europe Ben Amor et al. 2011; Caldwell and Vincent 2012; Filiz 2. Test for diferences in population structure and behav- and Taskavak 2012; Gristina et al. 2015), there is some con- iour throughout the range sensus for a conservative view of seahorse taxonomy. Some 3. Test for the correlation of population structure and mor- reports also suggest range extensions into European waters phology with environmental variables by non-native species: H. algiricus presence in the Canary Islands (Otero-Ferrer et al. 2015b, 2017), the Lessepsian This information will help to advance our ability to efec- migrant H. fuscus in the eastern Mediterranean (Golani and tively manage Hippocampus spp. within Europe, by provid- Fine 2002), and occasional rare migrants (e.g. H. erectus, ing detailed information that can help determine appropriate Woodall et al. 2009). Therefore genetic data are particularly protection and mitigation interventions as well as the accu- useful to clarify taxonomy and complement morphological rate assessment of seahorse populations. data (Padial et al. 2010). The two European seahorses H. guttulatus and H. hip- pocampus are the currently recognised names used in the Materials and methods IUCN Red List of Threatened Species (2012) and both are currently assessed as Data Defcient (Woodall 2012a, b). Geographic extent, literature sources Both species have a large geographic range extending across and standardization most of Europe and North Africa including the Atlantic Ocean, Mediterranean and Black Seas (Lourie et al. 1999b; The geographic extent of this review covers seahorse pop- Otero-Ferrer et al. 2017). Neither species is thought to be ulations from the Northeast Atlantic Ocean, including the 1 3 Marine Biology (2018) 165:19 Page 3 of 19 19 Macaronesian islands, and the Mediterranean and Black New sample acquisition and genetic analysis Seas. In total, data from 13 countries and 37 diferent sites are reviewed. These data cover the known geographic Most specimen tissue was collected during sampling dives. range of H. guttulatus and H. hippocampus (Lourie et al. Further specimens or tissue and associated data were also
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